Metazoan parasite fauna of detritivorous and omnivorous fishes from Amapá Lake, in western Brazilian Amazon

Negreiros, Luciano Pereira; Couto, João Victor; Tavares-Dias, Marcos

doi:10.1590/1676-0611-BN-2023-1571

Abstract

Despite being an important component of the freshwater ecosystems and an important factor controlling wild fish populations, Amazonian fish parasites have been poorly studied. Here, we analyzed the fauna of metazoan parasites from 10 detritivorous and omnivorous fish species from Amapá Lake in the western Amazon. Of 159 fish specimens examined, 73.6% were parasitized by one or more species of metazoan parasites. A total of 5,260 parasites (24 Monogenea, 14 Nematoda, 10 Digenea, 2 Acanthocephala, and 6 Crustacea) were identified. Aggregated dispersion pattern of parasites was observed. There was a predominance of endohelminth species that presented a similar pattern regarding the level of component communities (i.e., a low species number, low diversity and dominance of a single species, mainly the digeneans and nematodes in their larval stages). Five species of parasites presented correlation with the body size of the hosts. In the fish community, the presence of endoparasites in the larval and adult stages suggests that these are intermediate, paratenic and definitive hosts, reflecting their detritivorous or omnivorous feeding habits. The trophic level and diet had an influence on the structuring of endohelminth communities and infracommunities. Lastly, 38% of the metazoan parasite species were new records for examined hosts.

Keywords
Diet; freshwater fish; infection; parasites

Resumo

Apesar de ser um importante componente dos ecossistemas de água doce e um importante fator controlador das populações naturais de peixes, os parasitos de peixes amazônicos ainda são pouco estudados. Foi analisada a fauna de parasitos metazoários em 10 espécies de peixes detritívoros e onívoros do Lago Amapá na Amazônia ocidental. Dos 159 espécimes de peixes examinados, 73,6% estavam parasitados por uma ou mais espécies de parasitos metazoários. Um total de 5.260 parasitos (24 Monogenea, 14 Nematoda, 10 Digenea, 2 Acanthocephala e 6 Crustacea) foram identificados. Houve um padrão de dispersão agregado de parasitos. Houve predominância de espécies de endohelmintos que apresentaram padrão semelhante quanto ao nível de comunidades componentes, ou seja, baixo número de espécies, baixa diversidade e dominância de uma única espécie, principalmente os digenéticos e nematoides em estágio larval. Cinco espécies de parasitos apresentaram correlação com o tamanho corporal dos hospedeiros. Na comunidade de peixes, a presença de endoparasitos em fase larval e adulta sugere que esses são hospedeiros intermediários, paratênicos e definitivos, refletindo seus hábitos alimentares detritívoros ou onívoros. O nível trófico e dieta influenciaram na estruturação das comunidades e infracomunidades de endohelmintos. Por fim, 38% das espécies de parasitos metazoários foram novos registros para os hospedeiros examinados.

Palavras-chave
Dieta; infecção; parasitos; peixes de água doce

Introduction

Amapá Lake is located on the right bank of the Acre River and is 10 km from the city of Rio Branco, in the state of Acre (Brazil), in the southwestern Amazon region (10^o02’043.5”S and 67^o51’18.2”W), where horseshoe-shaped lakes are common. This lake was formed more than 40 years ago by an abandoned meandering of the Acre River. The lake is, therefore, isolated from the Acre River during the entire dry season, being connected with this river only during the flood season. It is an open and slightly deep body of water, about six km long with rich fauna and flora, and its margins are completely surrounded by dense tropical forest (^{Rodríguez-Zorro et al. 2015}27 RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
https://doi.org/10.1016/j.jsames.2015.06... ). From July to December, the lake remains hydrologically isolated from the main river channel. However, a connection is established when the river level exceeds 380 cm, thus surpassing the levee and flowing into the lake. This high-water period generally begins in January and lasts five to six months (^{Silva et al. 2013}29 SILVA, M.T, PEREIRA J.O., SOARES VIEIRA L.J. & PETRY, A.C. 2013. Hydrological seasonality of the river affecting fish community structure of oxbow lakes: A limnological approach on the Amapá Lake, southwestern Amazon. Limnologica 43:79–90. http://dx.doi.org/10.1016/j.limno.2012.05.002
https://doi.org/10.1016/j.limno.2012.05.... , ^{Rodríguez-Zorro et al. 2015}27 RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
https://doi.org/10.1016/j.jsames.2015.06... ). More than sixty zooplankton species such as Rotifera, Cladocera and Cyclopoida have been found in this lake (^{Keppeler 2003}11 KEPPELER, E.C. 2003. Abundance of zooplankton from different zones (pelagic and littoral) and time periods (morning and night) in two Amazonian meandering lakes. Acta Sci. Biol. Sci. 25(2):287–297., ^{Keppeler & Hardy 2004}12 KEPPELER, E.C. &. HARDY, E.R. 2004. Vertical distribution of zooplankton in the water column of Lago Amapá, Rio Branco, Acre State, Brazil. Rev. Brasil. Zool. 21(2):169–177. doi: 10.1590/S0101-81752004000200002
https://doi.org/10.1590/S0101-8175200400... , ^{Keppeler et al. 2018}13 KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.). The lake, in addition to receiving the load of material in suspension from the forming river, at the time of the decennial floods, it undergoes silting and eutrophication processes resulting from human action. Among these actions are the predatory fishing, deforestation, the opening of an unpaved road, as well as the disordered occupation of its margins (^{Rodríguez-Zorro et al. 2015}27 RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
https://doi.org/10.1016/j.jsames.2015.06... , ^{Keppeler et al. 2018}13 KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.). More than a hundred families live in the area surrounding Amapá Lake.

This lake presents an ichthyofauna comprised of 53 species of 18 families and five orders, with predominance of small and medium-size fishes that have socioenvironmental importance, especially for local fishing (^{Pereira et al. 2011}25 PEREIRA, J. O., SILVA M. T., VIEIRA L.J.S & FUGI, R. 2011. Effects of flood regime on the diet Triportheus curtus (Garman, 1890) in an Amazonian floodplain lake. Neotrop. Ichthyol. 9(3):623–628. doi: 10.1590/S1679-62252011005000029
https://doi.org/10.1590/S1679-6225201100... , ^{Silva et al. 2013}29 SILVA, M.T, PEREIRA J.O., SOARES VIEIRA L.J. & PETRY, A.C. 2013. Hydrological seasonality of the river affecting fish community structure of oxbow lakes: A limnological approach on the Amapá Lake, southwestern Amazon. Limnologica 43:79–90. http://dx.doi.org/10.1016/j.limno.2012.05.002
https://doi.org/10.1016/j.limno.2012.05.... ). Among these diverse species of fish are some Siluriformes and Characiformes. However, no study about the parasitic fauna in fish species from Amapá Lake is known. The parasites of Pimelodus blochii Valenciennes, 1840 (^{Negreiros et al. 2018}19 NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
https://doi.org/10.1007/s00436-018-6082-... ), Calophysus macropterus Lichtenstein, 1819 (^{Negreiros et al. 2019}20 NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
https://doi.org/10.1080/00222933.2019.16... ) from the Acre River, as well as diverse fish species from rivers Juruá, Crôa, Paranã, Gama and Santa Rosa, in the state of Acre have been reported (^{Virgilio et al. 2022}35 VIRGILIO, L.R., MARTINS, W.M.O., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. (2022). Endoparasite fauna of freshwater fish from the upper Juruá River in the Western Amazon, Brazil. J. Helminthol. 96: e55, 1–27. https://doi.org/10.1017/S0022149X2200027X
https://doi.org/10.1017/S0022149X2200027... ).

Parasites represent important components of global biodiversity in the ecosystems which have been neglected numerically and functionally for long time; despite them providing important information on the influence of environmental variation on species richness and diversity of parasites in the population distribution of hosts (^{Negreiros et al. 2019}20 NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
https://doi.org/10.1080/00222933.2019.16... , ^{Paterson et al. 2021}23 PATERSON, R.A., VIOZZI, G.P., RAUQUE, C.A., FLORES, V.R. & POULIN, R. A global Assessment of parasite diversity in galaxiid fishes. Diversity 13:27, 2021. https://doi.org/ 10.3390/d13010027
https://doi.org/10.3390/d13010027... , ^{Virgílio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.). Parasites can be also important agents of selection on wild host populations, affecting host fitness through effects on host growth, reproduction and survival (^{Tavares-Dias et al. 2017}32 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A., NEVES, L.R. 2017. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amaz. 47(2):155–162. https://doi.org/10.1590/1809-4392201602514
https://doi.org/10.1590/1809-43922016025... , ^{Virgílio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.). Due to the predominantly negative attention parasites receive, it is unsurprising that free-living species, as host fish, have received greater biodiversity conservation attention than the parasite species they harbor. However, understanding which factors drive differences in parasite diversity in wild fish populations has long been of great interest in fish parasitology (^{Paterson et al. 2021}23 PATERSON, R.A., VIOZZI, G.P., RAUQUE, C.A., FLORES, V.R. & POULIN, R. A global Assessment of parasite diversity in galaxiid fishes. Diversity 13:27, 2021. https://doi.org/ 10.3390/d13010027
https://doi.org/10.3390/d13010027... ).

Amazonian wild fish populations can generally harbor ectoparasites and endoparasites of diverse taxa, which display a variety of strategies in direct or indirect their life cycle. Freshwater fish of this Neotropical region can be parasitized by several taxa of metazoans in larval and adult stages (^{Karling et al. 2013}10 KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316., ^{Tavares-Dias et al. 2014}30 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
https://doi.org/10.2478/s11686-014-0225-... , ^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... , ^{Negreiros et al. 2018}19 NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
https://doi.org/10.1007/s00436-018-6082-... , ^{Negreiros et al. 2019}20 NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
https://doi.org/10.1080/00222933.2019.16... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... , ^{Virgilio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.). These parasites, particularly endohelminths, have life cycles that involve transmission through a trophic web of intermediate, paratenic and definitive hosts (^{Karling et al. 2013}10 KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316.; ^{Baia et al., 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... , ^{Virgilio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116., ^{Virgilio et al. 2022}35 VIRGILIO, L.R., MARTINS, W.M.O., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. (2022). Endoparasite fauna of freshwater fish from the upper Juruá River in the Western Amazon, Brazil. J. Helminthol. 96: e55, 1–27. https://doi.org/10.1017/S0022149X2200027X
https://doi.org/10.1017/S0022149X2200027... ). Hence, endohelminths can provide information regarding trophic interactions because their complex life cycle requires multiple hosts. The aim of study was to investigate the fauna of metazoan parasites in 10 detritivorous and omnivorous fish species from the Amapá Lake, in the State of Acre (Brazil). These fish species that occur in greater abundance in Amapá Lake.

Material and Methods

From December 2019 to December 2021, 10 fish species (Table 1) were collected in Lake Amapá (Figure 1), in the municipality of Rio Branco, in the State of Acre (Brazil). The fish were packed on ice and transported to the Multidisciplinary Laboratory of the Acre Federal Institute (IFAC), in Rio Branco (Brazil). Each fish was weighed (g) and measured in total length (cm), and analyzed for parasites. The gills, eyes, viscera and gastrointestinal tract of each fish were examined for the presence of metazoan parasites. The parasites were collected, fixed, preserved and prepared for identification according to the methods suggested by ^{Eiras et al. (2006)}8 EIRAS, J.C., TAKEMOTO, R.M. & PAVANELLI, G.C. 2006. Métodos de estudos e técnicas laboratoriais em parasitologia de Peixes. Eduem, Maringá, 199p.. To identify the parasites, previous recommendations were used (^{Moravec 1998}18 MORAVEC, F. 1998. Nematodes of freshwater fishes of the Neotropical region. Praha, Vydala Academia, 464 p., ^{Thatcher 2006}33 THATCHER, V.E. Amazon Fish Parasites. Pensoft: Sofia Moscow., ^{Kohn et al. 2007}14 KOHN, A., FERNANDES, B.M.M. & COHEN, S.C. 2007. South American trematodes parasites of fishes. Imprinta Express Ltda, Rio de Janeiro., ^{Cohen et al. 2013}5 COHEN, S.C., JUSTO, M.C.N. & KOHN. 2013. South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro: Oficina de Livros., ^{Rigby 2014}26 RIGBY, M.C. 2014. 7.20 Order Camallanida: Superfamilies Anguillicoloidea and Camallanoidea. In: SCHMIDT-RHAESA, A (Ed.) Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera: Vol. 2, Nematoda. Walter De Gruyter, Berlin, p. 637–659.).

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Table 1.
Body parameters of fish from Amapá Lake, in western Amazon (Brazil).

Figure 1.
Collection site of the fish in Amapá Lake, in western Amazon (Brazil).

Prevalence, mean intensity, and mean abundance were used to describe parasite infection parameters (^{Bush et al. 1997}3 BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. & SHOSTAK. W. 1997.Parasitology meets ecology on its own terms, Margolis et al. revisited. J. Parasitol. 83:575–583.). The dispersion index (ID) and Poulin discrepancy index (D) were calculated using the Quantitative Parasitology 3.0 software to detect the distribution pattern of each parasite infracommunity with a prevalence >10% (^{Rózsa et al. 2000)}28 RÓZSA, L., REICZIGEL, J. & MAJOROS, G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86:228–232.. The significance of the ID for each parasite infracommunity was tested using the d-statistical test (^{Ludwig & 1988}15 LUDWIG, J.A. & REYNOLDS, J.F. 1988. Statistical ecology, a primer on methods and computing. New York, Wiley-Interscience Pub.). Spearman’s correlation coefficient (rs) was used to determine possible correlations between the abundance of parasites and the length and weight of host fish (^{Zar 2010}37 ZAR, J.H. 2010. Biostatistical analysis. 5th ed. Prentice Hall, New Jersey.).

This study was approved by the Ethics Committee for the Use of Animals at Embrapa Amapá (Protocol N^o 014/2018 – CEUA/CPAFAP).

Results

A total of 159 specimens of four species of detritivorous and six omnivorous fish were examined (Table 1).

The host fish were parasitized by 56 taxa of metazoan parasites: 24 species of Monogenea, 14 species of Nematoda, 2 Acanthocephala, 10 Digenea and 6 Crustacea. Of the 159 fish examined, 73.6% (N = 117) were parasitized by one or more species of metazoan parasites. A total of 5,260 parasites were recovered mostly of the gills and intestine of the host fish. Prevalence, mean intensity and mean abundance of the parasites varied between the host species examined (Table 2).

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Table 2.
Metazoan parasites in fish species from Amapá Lake, in western Amazon (Brazil).

The parasites of Potamorhina latior Spix & Agassiz, 1829 and Hypophthalmus marginatus Valenciennes, 1840 showed an aggregated dispersion pattern, and in some infracommunities this pattern was highly aggregated (Table 3).

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Table 3.
Dispersion index (DI), d-statistic (d), and discrepancy index (D) for the infracommunity of metazoan parasites in fish species from Amapá Lake, in western Amazon (Brazil).

A positive correlation of Proterodiplostomidae gen. sp. abundance with the body length of Curimata inornata Vari, 1989, and a negative correlation with the body length and weight of P. latior was found. A positive correlation of monogenean abundance with the body weight, as well as of the Miracetyma sp. abundance with the length of H. marginatus was observed. There is also a positive correlation of abundance of Notozothecium lamotherargumedoi Cohen & Kohn, 2008 with the length of Rhaphiodon vulpinus Spix & Agassiz, 1829 (Table 4).

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Table 4.
Spearman correlation coefficient (rs) of the abundance of metazoan parasites with the length and weight of fish species from Amapá Lake, in western Amazon (Brazil).

Discussion

Host fish species of Amapá Lake occupying same trophic niche, but consuming different food items and presenting divergent feeding behavior, were exposed to different parasite species and had different parasite diversity, resulting in differences in the infection patterns. In parasites infracommunity level, these host fish showed a variation in the prevalence, intensity and abundance. Differences in exposure to parasites may have led to these divergences among sympatric host fish, which have differenced immunity. In addition, in P. latior and H. marginatus, an aggregated pattern of the parasites was found, and the level of aggregation varied between parasite species. In freshwater fish species, aggregated distribution of parasites is a common pattern and potentially influenced by factors related to parasites and host fish (^{Tavares-Dias et al. 2014}30 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
https://doi.org/10.2478/s11686-014-0225-... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). This distribution pattern of parasites indicates that either some fish are more attractive to the parasites or the infection is patchy, or both. Therefore, aggregated parasitic loads appear to be largely controlled by differences in opportunity for infection to occur that result from spending different amounts of time in vicinity of a hotspot of infection.

We found that the metazoan parasite communities of the 10 species of detritivorous and omnivorous fish here examined consisted of monogeneans, nematodes, acanthocephalans, digeneans and crustaceans, but with a dominance by monogeneans. However, some of the helminths were in the larval stages, including nematodes (24%), digeneans (18%) and acanthocephalans species (4.0%); hence, the predominance was of endoparasites in larval stage. This suggests that the host fish play an important role in the transmission dynamics of these endoparasites (^{Pavanelli et al. 2004}24 PAVANELLI, G.C., MACHADO, M.H., TAKEMOTO, R.M., GUIDELLI, G.M. & LIZAMA, M.A.P. 2004. Helminth fauna of fishes: Diversity and ecological aspects. In THOMAZ, SM., AGOSTINHO, AA. & HAHN, NS. The upper Paraná River and its floodplain physical aspects, ecology and conservation. Backhuys Publishers: Leiden. p. 309–329., ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). In the food web, the trophic level of populations host fish may be a good indicator regarding these hosts’ exposure to parasites. In addition, the endohelminths presented a similar pattern regarding the level of component communities (i.e., a low species number, low diversity and dominance of a single species, mainly the digeneans and nematodes in larval stage). The endohelminth communities of an assemblage of omnivorous and piscivorous fish of Matapi River, a tributary of Amazon River system in northern Brazil, also presented a similar pattern regarding the component community level, i.e. a low number of species, low diversity and dominance of a single species, mainly nematode species (^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). In an assemblage of detritivorous, carnivorous, omnivorous and piscivorous fish of a tributary from the Amazon River system in northern Brazil, the predominance was also of nematode species in larval stage (^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... ). However, in an assemblage of detritivorous, omnivorous and piscivorous fish Juruá River system, a tributary of the Amazon River in northern Brazil, the predominance was of nematode and cestode species (^{Virgilio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.). Therefore, these characteristics seem to be adaptations to the food web and to the high densities of organisms distributed over wide spatial scales that are common in Amazonian ecosystems (^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). The knowledge on the benthic and zooplankton species in these Amazonian ecosystems could provide information that are fundamental to explaining these compositions of the endohelminth fauna in these assemblages of host fish. Amapá Lake has more than sixty zooplankton species (^{Keppeler 2003}11 KEPPELER, E.C. 2003. Abundance of zooplankton from different zones (pelagic and littoral) and time periods (morning and night) in two Amazonian meandering lakes. Acta Sci. Biol. Sci. 25(2):287–297., ^{Keppeler & Hardy 2004}12 KEPPELER, E.C. &. HARDY, E.R. 2004. Vertical distribution of zooplankton in the water column of Lago Amapá, Rio Branco, Acre State, Brazil. Rev. Brasil. Zool. 21(2):169–177. doi: 10.1590/S0101-81752004000200002
https://doi.org/10.1590/S0101-8175200400... , ^{Keppeler et al. 2018}13 KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.), in addition to invertebrates as crustaceans and mollusks. Almost all digeneans uses mollusks as first intermediate host in their life cycle. Nematodes also have complex life cycle involving several intermediate hosts, and their first intermediate hosts are nearly always invertebrates of the zooplankton fauna, particularly copepod species. Thus, surveys about the fauna of invertebrates may explain the compositions of the endohelminths in assemblages of host fish, because these parasites are transmitted to fish by predation of invertebrates, which are the primary intermediate hosts (^{Pavanelli et al. 2004}24 PAVANELLI, G.C., MACHADO, M.H., TAKEMOTO, R.M., GUIDELLI, G.M. & LIZAMA, M.A.P. 2004. Helminth fauna of fishes: Diversity and ecological aspects. In THOMAZ, SM., AGOSTINHO, AA. & HAHN, NS. The upper Paraná River and its floodplain physical aspects, ecology and conservation. Backhuys Publishers: Leiden. p. 309–329., ^{Karling et al., 2013}10 KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316.; ^{Mbokane et al. 2015}17 MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
https://doi.org/10.1515/helmin-2015-0037... , ^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). Thus, the presence of intermediate hosts in the aquatic environment may explain the abundance and diversity of the endoparasites of a certain region. The feeding habit of the host fish populations is one of the most relevant factors explaining the composition of the endoparasite species in this study, which hosts have different feeding habit.

In host fish, in addition to adaptations to environmental factors, specific adaptations to parasitic mode of life may lead to restriction of infections. These parasite-host interactions are generally characterized by highly complex processes. In host-parasite networks, the host fish body provides a microhabitat for parasite species of different taxa and with different life history and strategies attachment (^{Tavares-Dias et al. 2015}31 TAVARES-DIAS, M., DIAS-JÚNIOR, M.B.F., FLORENTINO, A.C., SILVA, L.M.A. & CUNHA, AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev. Bras. Parasitol. Vet. 24:136–147. https://doi.org/10.1590/S1984-29612015036
https://doi.org/10.1590/S1984-2961201503... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... , ^{Oliveira et al. 2022}22 OLIVEIRA, M.S.B., PRESTES, L., ADRIANO, E.A., TAVARES-DIAS, M. 2022. Morphological and functional structure of two Ergasilidae parasites determine their microhabitat affinity on the gills of an Anostomidae fish from the Amazon. Parasitol. Res. 121:2295–2305: https://doi.org/10.1007/s00436-022-07569-6
https://doi.org/10.1007/s00436-022-07569... ). In this study, host-endoparasite interaction showed that the host fish provided a microhabitat, typically the intestine, for more than two third species of endohelminths which have different developmental strategies; mostly R. vulpinus, H. marginatus and Pimelodus blochii Valenciennes, 1840. In addition, there was a moderate diversity of endohelminths associated with each host species, as microhabitats are limited environments and because even susceptible host species are unable to harbor all of the parasites in a network. Although some host fish have the same feeding habits, they differ in body size and immune system, factors that restrict interactions between many parasite species (^{Bellay et al. 2013}2 BELLAY, S., OLIVEIRA, E.F., ALMEIDA-NETO, M., LIMA, J., PEREIRA, D., TAKEMOTO, R.M. & LUQUE JL. 2013. Developmental stage of parasites influences the structure of fish-parasite networks. PlosOne 8: e75710. Doi: 10.1371/journal.pone.0075710
https://doi.org/10.1371/journal.pone.007... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). Due to the complex relationship between parasites and the environment, initially the parasite attempts to establish itself in the host fish while the latter resist the infection via its defense mechanisms. Consequently, host susceptibility and resistance will determine whether the infection becomes established or not (^{Tavares-Dias et al. 2017}32 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A., NEVES, L.R. 2017. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amaz. 47(2):155–162. https://doi.org/10.1590/1809-4392201602514
https://doi.org/10.1590/1809-43922016025... ). Variations in infection patterns also may be related to several biotic and abiotic factors (^{Tavares-Dias et al. 2014}30 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
https://doi.org/10.2478/s11686-014-0225-... , ^{Karling et al. 2013}10 KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316., ^{Mbokane et al. 2015}17 MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
https://doi.org/10.1515/helmin-2015-0037... , ^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... , ^{Negreiros et al. 2018}19 NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
https://doi.org/10.1007/s00436-018-6082-... , ^{Negreiros et al. 2019}20 NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
https://doi.org/10.1080/00222933.2019.16... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). However, Psectrogaster rutiloides Kner, 1858 from Amapá Lake was the single host uninfected among the examined host species, because only eight fish were examined.

Amapá Lake, in addition to receiving the load of material in suspension from the forming river, at the time of the decennial floods, it also undergoes silting and eutrophication processes resulting from anthropogenic action (^{Rodríguez-Zorro et al. 2015}27 RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
https://doi.org/10.1016/j.jsames.2015.06... , ^{Keppeler et al. 2018}13 KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.). Hence, monogenean species which are ectoparasites with simple and direct life cycle and that are present mainly in eutrophized and lentic environments (^{Dogiel 1961}7 DOGIEL, V.A. 1961. Ecology of the parasites of freshwater fishes. In: DOGIEL, V.A.; PETRUSHEVSKI, G.K.; POLYANSKI, Y.I. (Ed.). Parasitology of fishes. University Press: Leningrad, p.1–47., ^{Pavanelli et al. 2004}24 PAVANELLI, G.C., MACHADO, M.H., TAKEMOTO, R.M., GUIDELLI, G.M. & LIZAMA, M.A.P. 2004. Helminth fauna of fishes: Diversity and ecological aspects. In THOMAZ, SM., AGOSTINHO, AA. & HAHN, NS. The upper Paraná River and its floodplain physical aspects, ecology and conservation. Backhuys Publishers: Leiden. p. 309–329., ^{Cunha et al. 2021}6 CUNHA, K.N., DOMINGUES, M.V., CUNHA, L.D.S. & NUNES, Z.M.P. 2021. Parasitic monogenoideans of Sciades herzbergii as bioindicators of environmental quality in Amazonian estuarines ecosystems. Rev. Brasil. Parasitol. Vet. 30(1):e024220. https://doi.org/10.1590/S1984-29612021013
https://doi.org/10.1590/S1984-2961202101... ), were collected in 66.7% of the examined host fish. Metacercariae of digeneans were found in C. inornata, P. latior, R. vulpinus, A. nuchalis, H. marginatus, Nemadoras humeralis Kner, 1855, P. blochii and Sorubim lima Bloch & Schneider, 1801, which are intermediate hosts for these endoparasites with complex life cycle. Larvae of acanthocephalans were recovered only of H. marginatus. Nematode larvae, mostly anisakid species, were found in P. latior, R. vulpinus, H. marginatus, N. humeralis, P. blochii and S. lima, which are secondary intermediate hosts for these endoparasites. Lentic ecosystems provide specific conditions, such as a higher water temperature and lower water currents, which facilitates concentration of the first and secondary intermediate hosts, thus increasing the probability of the cercariae of digeneans (^{Mbokane et al. 2015}17 MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
https://doi.org/10.1515/helmin-2015-0037... ) and larvae of nematodes to locate its hosts. In addition, these conditions make the secondary intermediate hosts more vulnerable to predation by fish-eating birds, which are definitive hosts for some endohelminths species. Endohelminths in larval stages have been also reported for assemblage of omnivorous and piscivorous fish of Matapi River (^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ), as well as for assemblage of detritivorous, carnivorous, omnivorous and piscivorous fish from Igarapé Fortaleza River (^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... ), due to presence of infective stages in these Amazonian environments.

Pimelodus blochii from Amapá Lake presented a community of endoparasites lower than reported for this same host of rivers Acre and Iaco in western Amazon (^{Negreiros et al. 2018}19 NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
https://doi.org/10.1007/s00436-018-6082-... ). Curimatella meyeri Steindachner, 1882 was infected only by monogeneans while this same host from Juruá River was parasitized by Cosmoxynema vianai Travassos, 1949 and unidentified Cladorchiidae (^{Virgilio et al. 2021}34 VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.). These divergences in parasitofauna are influenced by the distinct environments of host fish. However, the community of endoparasites in R. vulpinus was similar to this same host of floodplain from upper Paraná River (^{Karling et al. 2013}10 KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316.), as well as the monogenean fauna of hosts of lakes from the State of Amazonas (^{Morey & Malta, 2018}16 MOREY, G.A.M. & MALTA, J.C.O. 2018. Monogenoideans parasitizing Rhaphiodon vulpinus Spix & Agassiz, 1829 (Characiformes: Cynodontidae) from Lakes Baixio and Catalão, Amazonas, Brazil. Neotrop. Helminthol. 12(1):21–26.). Third-stage larvae of Contracaecum sp., Terranova sp. and Anisakidae gen. sp. were found in H. marginatus of this study. However, for this same host from Tocantins River, larvae of third-stage of Hysterothylacium sp. and Anisakis sp. has been reported (^{Cárdenas et al. 2021}4 CÁRDENAS, M.Q., JUSTO, M.C.N, VIANA, D.C. & SIMONE CHINICZ COHEN, S.C. 2021. New host record and geographical distribution of Nematoda parasitizing Hypophthalmus marginatus Valenciennes (Siluriformes) from the Tocantins River, Brazil. Acta Sci. Biol. Sci 43:e58014. Doi: 10.4025/actascibiolsci.v43i1.58014.
https://doi.org/10.4025/actascibiolsci.v... ).

A wide diversity of parasite crustacean species infests wild fish populations, and these can attack the gills, oral cavity, nostrils and/or skin of the hosts. Microhabitat in the gills, and the physical attributes of crustacean ectoparasites, have been proposed as causal factors for the distribution of host fish populations. It has been suggested that attachment site specificity is result of the need to avoid interspecific competition for space and food (^{Oliveira et al. 2022}22 OLIVEIRA, M.S.B., PRESTES, L., ADRIANO, E.A., TAVARES-DIAS, M. 2022. Morphological and functional structure of two Ergasilidae parasites determine their microhabitat affinity on the gills of an Anostomidae fish from the Amazon. Parasitol. Res. 121:2295–2305: https://doi.org/10.1007/s00436-022-07569-6
https://doi.org/10.1007/s00436-022-07569... ). Crustaceans are ectoparasites that can exhibit host specificity and interspecific variations, as well as affinity of microhabitat in the host fish (^{Tavares-Dias et al. 2015}31 TAVARES-DIAS, M., DIAS-JÚNIOR, M.B.F., FLORENTINO, A.C., SILVA, L.M.A. & CUNHA, AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev. Bras. Parasitol. Vet. 24:136–147. https://doi.org/10.1590/S1984-29612015036
https://doi.org/10.1590/S1984-2961201503... , ^{Williams & Bunkley-Williams 2019}36 WILLIAMS, E.H. & BUNKLEY-WILLIAMS, L. 2019. Life Cycle and life history strategies of parasitic Crustacea. In: SMIT, N., BRUCE, N. & HADFIELD, K. (eds). Parasitic Crustacea. Zoological Monographs, vol 3. Springer, p 179–266., ^{Oliveira et al., 2022}22 OLIVEIRA, M.S.B., PRESTES, L., ADRIANO, E.A., TAVARES-DIAS, M. 2022. Morphological and functional structure of two Ergasilidae parasites determine their microhabitat affinity on the gills of an Anostomidae fish from the Amazon. Parasitol. Res. 121:2295–2305: https://doi.org/10.1007/s00436-022-07569-6
https://doi.org/10.1007/s00436-022-07569... ). Ergasilus jaraquensis Thatcher & Robertson, 1982 occurred in C. inornata, Miracetyma etimaruya Malta, 1993 occurred in P. latior, Miracetyma kawa Malta, 1994 infested R. vulpinus, Miracetymasp. was found in H. marginatus, Ergasilus sp. infested P. blochii and Isopoda unidentified infested Nemadoras humeralis Kner, 1855. These parasites were found attached in the gills of host fish, and in low infestation levels, except Miracetymasp., which had a high prevalence and moderate intensity and abundance.

The body size of host fish can be another factor influencing the structure of infracommunities of parasites; however, this factor explains only part of the variation in parasite abundance, because other factors than host body size are more important determinants of this variation (^{Tavares-Dias et al. 2014}30 TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
https://doi.org/10.2478/s11686-014-0225-... , ^{Mbokane et al. 2015}17 MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
https://doi.org/10.1515/helmin-2015-0037... , ^{Baia et al. 2018}1 BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
https://doi.org/10.1515/ap-2018-0035... , ^{Negreiros et al. 2019}20 NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
https://doi.org/10.1080/00222933.2019.16... , ^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). In C. inornata, the abundance of metacercariae of digeneans increased with host body size; contrarily, in P. latior decreased with increase in weight and length of the hosts. In R. vulpinus, the abundance of monogeneans increased with host length, while in H. marginatus the abundance of monogeneans increased with host weight. These results suggest a variation in the feeding behavior of these fish in different age (^{Neves et al. 2021}21 NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
https://doi.org/10.1007/s11686-021-00413... ). Considering the complexity of these involved factors, further investigations need to be carried out in the future for a better understanding the influence of these factors in determining variation on parasite abundance.

In conclusion, data of the present study revealed interactions and importance on the parasite-hosts of an Amazonian lake. The metazoan parasites fauna was composed of different species and showed a dominance of monogeneans followed by nematodes > digeneans > crustaceans > acanthocephalans. The present study also revealed that 38% of the metazoan parasite species were new records for the different hosts examined. Endoparasites were found in the larval and adult stages, suggesting that these fish are intermediate, paratenic and definitive hosts, providing the basis for the development of these organisms and intermediating the way to their definitive hosts. Parasite-host interaction network reflected the detritivorous and omnivorous feeding habits of the sampled fish species, some of which are prey for other fish that are top of web. The size of the host fish had influence on the structuring of parasites infracommunities, but the trophic level and diet also had an influence. This epidemiological survey is the first attempt to understand patterns and processes of parasitic infections in wild fish populations in a lake of abandoned meandering in Amazon. Considering the complexity of the Amapá Lake, other investigations need to be conducted in the future for a better understanding of other factors that may determine the patterns and processes in the acquisition of parasite species. Lastly, this study established diversity and infection data for the metazoan parasite fauna of some fish species in the Amapá Lake, an ecosystem that is subject to increase in environmental changes due to agriculture activities, deforestation and urbanization. Therefore, these data could be used for comparisons in future studies regarding environmental anthropogenic impacts in this lake.

Acknowledgements

Marcos Tavares-Dias was supported by a research fellowship from the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq, Brazil) (Grant 301911/2022-3). The authors thank to Dr. Hudson Alves Pinto from UFMG for help in identification of digeneans and to Dr. Felipe Bisaggio Pereira from UFMG for help in identification of nematodes.

Data Availability

Records of specimens of 10 fish species with the respective measurements (weight and length) and taxonomic identification, location, collecting date and abundance of parasites. https://data.scielo.org/file.xhtml?fileId=5611&version=DRAFT

References

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BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
» https://doi.org/10.1515/ap-2018-0035
²
BELLAY, S., OLIVEIRA, E.F., ALMEIDA-NETO, M., LIMA, J., PEREIRA, D., TAKEMOTO, R.M. & LUQUE JL. 2013. Developmental stage of parasites influences the structure of fish-parasite networks. PlosOne 8: e75710. Doi: 10.1371/journal.pone.0075710
» https://doi.org/10.1371/journal.pone.0075710
³
BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. & SHOSTAK. W. 1997.Parasitology meets ecology on its own terms, Margolis et al. revisited. J. Parasitol. 83:575–583.
⁴
CÁRDENAS, M.Q., JUSTO, M.C.N, VIANA, D.C. & SIMONE CHINICZ COHEN, S.C. 2021. New host record and geographical distribution of Nematoda parasitizing Hypophthalmus marginatus Valenciennes (Siluriformes) from the Tocantins River, Brazil. Acta Sci. Biol. Sci 43:e58014. Doi: 10.4025/actascibiolsci.v43i1.58014.
» https://doi.org/10.4025/actascibiolsci.v43i1.58014
⁵
COHEN, S.C., JUSTO, M.C.N. & KOHN. 2013. South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro: Oficina de Livros.
⁶
CUNHA, K.N., DOMINGUES, M.V., CUNHA, L.D.S. & NUNES, Z.M.P. 2021. Parasitic monogenoideans of Sciades herzbergii as bioindicators of environmental quality in Amazonian estuarines ecosystems. Rev. Brasil. Parasitol. Vet. 30(1):e024220. https://doi.org/10.1590/S1984-29612021013
» https://doi.org/10.1590/S1984-29612021013
⁷
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⁹
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» www.fishbase.org
¹⁰
KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316.
¹¹
KEPPELER, E.C. 2003. Abundance of zooplankton from different zones (pelagic and littoral) and time periods (morning and night) in two Amazonian meandering lakes. Acta Sci. Biol. Sci. 25(2):287–297.
¹²
KEPPELER, E.C. &. HARDY, E.R. 2004. Vertical distribution of zooplankton in the water column of Lago Amapá, Rio Branco, Acre State, Brazil. Rev. Brasil. Zool. 21(2):169–177. doi: 10.1590/S0101-81752004000200002
» https://doi.org/10.1590/S0101-81752004000200002
¹³
KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.
¹⁴
KOHN, A., FERNANDES, B.M.M. & COHEN, S.C. 2007. South American trematodes parasites of fishes. Imprinta Express Ltda, Rio de Janeiro.
¹⁵
LUDWIG, J.A. & REYNOLDS, J.F. 1988. Statistical ecology, a primer on methods and computing. New York, Wiley-Interscience Pub.
¹⁶
MOREY, G.A.M. & MALTA, J.C.O. 2018. Monogenoideans parasitizing Rhaphiodon vulpinus Spix & Agassiz, 1829 (Characiformes: Cynodontidae) from Lakes Baixio and Catalão, Amazonas, Brazil. Neotrop. Helminthol. 12(1):21–26.
¹⁷
MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
» https://doi.org/10.1515/helmin-2015-0037
¹⁸
MORAVEC, F. 1998. Nematodes of freshwater fishes of the Neotropical region. Praha, Vydala Academia, 464 p.
¹⁹
NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
» https://doi.org/10.1007/s00436-018-6082-5
²⁰
NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
» https://doi.org/10.1080/00222933.2019.1657195
²¹
NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
» https://doi.org/10.1007/s11686-021-00413-4
²²
OLIVEIRA, M.S.B., PRESTES, L., ADRIANO, E.A., TAVARES-DIAS, M. 2022. Morphological and functional structure of two Ergasilidae parasites determine their microhabitat affinity on the gills of an Anostomidae fish from the Amazon. Parasitol. Res. 121:2295–2305: https://doi.org/10.1007/s00436-022-07569-6
» https://doi.org/10.1007/s00436-022-07569-6
²³
PATERSON, R.A., VIOZZI, G.P., RAUQUE, C.A., FLORES, V.R. & POULIN, R. A global Assessment of parasite diversity in galaxiid fishes. Diversity 13:27, 2021. https://doi.org/ 10.3390/d13010027
» https://doi.org/10.3390/d13010027
²⁴
PAVANELLI, G.C., MACHADO, M.H., TAKEMOTO, R.M., GUIDELLI, G.M. & LIZAMA, M.A.P. 2004. Helminth fauna of fishes: Diversity and ecological aspects. In THOMAZ, SM., AGOSTINHO, AA. & HAHN, NS. The upper Paraná River and its floodplain physical aspects, ecology and conservation. Backhuys Publishers: Leiden. p. 309–329.
²⁵
PEREIRA, J. O., SILVA M. T., VIEIRA L.J.S & FUGI, R. 2011. Effects of flood regime on the diet Triportheus curtus (Garman, 1890) in an Amazonian floodplain lake. Neotrop. Ichthyol. 9(3):623–628. doi: 10.1590/S1679-62252011005000029
» https://doi.org/10.1590/S1679-62252011005000029
²⁶
RIGBY, M.C. 2014. 7.20 Order Camallanida: Superfamilies Anguillicoloidea and Camallanoidea. In: SCHMIDT-RHAESA, A (Ed.) Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera: Vol. 2, Nematoda. Walter De Gruyter, Berlin, p. 637–659.
²⁷
RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
» https://doi.org/10.1016/j.jsames.2015.06.003
²⁸
RÓZSA, L., REICZIGEL, J. & MAJOROS, G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86:228–232.
²⁹
SILVA, M.T, PEREIRA J.O., SOARES VIEIRA L.J. & PETRY, A.C. 2013. Hydrological seasonality of the river affecting fish community structure of oxbow lakes: A limnological approach on the Amapá Lake, southwestern Amazon. Limnologica 43:79–90. http://dx.doi.org/10.1016/j.limno.2012.05.002
» https://doi.org/10.1016/j.limno.2012.05.002
³⁰
TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
» https://doi.org/10.2478/s11686-014-0225-3
³¹
TAVARES-DIAS, M., DIAS-JÚNIOR, M.B.F., FLORENTINO, A.C., SILVA, L.M.A. & CUNHA, AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev. Bras. Parasitol. Vet. 24:136–147. https://doi.org/10.1590/S1984-29612015036
» https://doi.org/10.1590/S1984-29612015036
³²
TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A., NEVES, L.R. 2017. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amaz. 47(2):155–162. https://doi.org/10.1590/1809-4392201602514
» https://doi.org/10.1590/1809-4392201602514
³³
THATCHER, V.E. Amazon Fish Parasites. Pensoft: Sofia Moscow.
³⁴
VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.
³⁵
VIRGILIO, L.R., MARTINS, W.M.O., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. (2022). Endoparasite fauna of freshwater fish from the upper Juruá River in the Western Amazon, Brazil. J. Helminthol. 96: e55, 1–27. https://doi.org/10.1017/S0022149X2200027X
» https://doi.org/10.1017/S0022149X2200027X
³⁶
WILLIAMS, E.H. & BUNKLEY-WILLIAMS, L. 2019. Life Cycle and life history strategies of parasitic Crustacea. In: SMIT, N., BRUCE, N. & HADFIELD, K. (eds). Parasitic Crustacea. Zoological Monographs, vol 3. Springer, p 179–266.
³⁷
ZAR, J.H. 2010. Biostatistical analysis. 5th ed. Prentice Hall, New Jersey.

Edited by

Associate Editor

Juan Schmitter-Soto

Publication Dates

Publication in this collection
03 May 2024
Date of issue
2024

History

Received
26 Sept 2023
Accepted
11 Jan 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

[1] ¹
BAIA, R.R.J., FLORENTINO, A.C., SILVA, L.M.A. & TAVARES-DIAS, M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol. 63(2): 304–316. Doi: 10.1515/ap-2018-0035
» https://doi.org/10.1515/ap-2018-0035

[2] ²
BELLAY, S., OLIVEIRA, E.F., ALMEIDA-NETO, M., LIMA, J., PEREIRA, D., TAKEMOTO, R.M. & LUQUE JL. 2013. Developmental stage of parasites influences the structure of fish-parasite networks. PlosOne 8: e75710. Doi: 10.1371/journal.pone.0075710
» https://doi.org/10.1371/journal.pone.0075710

[3] ³
BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. & SHOSTAK. W. 1997.Parasitology meets ecology on its own terms, Margolis et al. revisited. J. Parasitol. 83:575–583.

[4] ⁴
CÁRDENAS, M.Q., JUSTO, M.C.N, VIANA, D.C. & SIMONE CHINICZ COHEN, S.C. 2021. New host record and geographical distribution of Nematoda parasitizing Hypophthalmus marginatus Valenciennes (Siluriformes) from the Tocantins River, Brazil. Acta Sci. Biol. Sci 43:e58014. Doi: 10.4025/actascibiolsci.v43i1.58014.
» https://doi.org/10.4025/actascibiolsci.v43i1.58014

[5] ⁵
COHEN, S.C., JUSTO, M.C.N. & KOHN. 2013. South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro: Oficina de Livros.

[6] ⁶
CUNHA, K.N., DOMINGUES, M.V., CUNHA, L.D.S. & NUNES, Z.M.P. 2021. Parasitic monogenoideans of Sciades herzbergii as bioindicators of environmental quality in Amazonian estuarines ecosystems. Rev. Brasil. Parasitol. Vet. 30(1):e024220. https://doi.org/10.1590/S1984-29612021013
» https://doi.org/10.1590/S1984-29612021013

[7] ⁷
DOGIEL, V.A. 1961. Ecology of the parasites of freshwater fishes. In: DOGIEL, V.A.; PETRUSHEVSKI, G.K.; POLYANSKI, Y.I. (Ed.). Parasitology of fishes. University Press: Leningrad, p.1–47.

[8] ⁸
EIRAS, J.C., TAKEMOTO, R.M. & PAVANELLI, G.C. 2006. Métodos de estudos e técnicas laboratoriais em parasitologia de Peixes. Eduem, Maringá, 199p.

[9] ⁹
FROESE, R., PAULY, D. Editors (2023) FishBase. World Wide Web electronic publication. www.fishbase.org, version (06/2023)
» www.fishbase.org

[10] ¹⁰
KARLING, L.C., LACERDA, A.C.F., ALVARENGA, F.M.S., TAKEMOTO, R.M. & PAVANELLI, G.C. 2013. Endoparasites of Rhaphiodon vulpinus (Characiformes: Cynodontidae) and their relation to the standard length and sex of their hosts. Biosci. J. 29(5):1311–1316.

[11] ¹¹
KEPPELER, E.C. 2003. Abundance of zooplankton from different zones (pelagic and littoral) and time periods (morning and night) in two Amazonian meandering lakes. Acta Sci. Biol. Sci. 25(2):287–297.

[12] ¹²
KEPPELER, E.C. &. HARDY, E.R. 2004. Vertical distribution of zooplankton in the water column of Lago Amapá, Rio Branco, Acre State, Brazil. Rev. Brasil. Zool. 21(2):169–177. doi: 10.1590/S0101-81752004000200002
» https://doi.org/10.1590/S0101-81752004000200002

[13] ¹³
KEPPELER, E.C., SERRA, A.J., VIEIRA, L.J.S., PEREIRA J.O., SILVA MT., SANTOS M.J.A. & FERRAUDO, A, S. 2018. Seasonal fluctuations of Rotifera in a tropical lake in Amazonia (Acre River floodplain, Brazil). Hidrobiologica 28(3):235–347.

[14] ¹⁴
KOHN, A., FERNANDES, B.M.M. & COHEN, S.C. 2007. South American trematodes parasites of fishes. Imprinta Express Ltda, Rio de Janeiro.

[15] ¹⁵
LUDWIG, J.A. & REYNOLDS, J.F. 1988. Statistical ecology, a primer on methods and computing. New York, Wiley-Interscience Pub.

[16] ¹⁶
MOREY, G.A.M. & MALTA, J.C.O. 2018. Monogenoideans parasitizing Rhaphiodon vulpinus Spix & Agassiz, 1829 (Characiformes: Cynodontidae) from Lakes Baixio and Catalão, Amazonas, Brazil. Neotrop. Helminthol. 12(1):21–26.

[17] ¹⁷
MBOKANE, E.M., THERON, J. & LUUS-POWELL, J.W. 2015. Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River system, South Africa. Helminthologia 52:229–235. https:// doi. org/10.1515/helmin-2015-0037
» https://doi.org/10.1515/helmin-2015-0037

[18] ¹⁸
MORAVEC, F. 1998. Nematodes of freshwater fishes of the Neotropical region. Praha, Vydala Academia, 464 p.

[19] ¹⁹
NEGREIROS, L.P., PEREIRA, F.B., TAVARES-DIAS, M., TAVARES, L.E.R. 2018. Community structure of metazoan parasites from Pimelodus blochii in two rivers of the Western Brazilian Amazon: same seasonal traits, but different anthropogenic impacts. Parasitol. Res. 117:3791–3798. https://doi.org/10.1007/s00436-018-6082-5
» https://doi.org/10.1007/s00436-018-6082-5

[20] ²⁰
NEGREIROS, L.P., PEREIRA, F.B. & TAVARES-DIAS, M. 2019. Metazoan parasites of Calophysus macropterus (Siluriformes: Pimelodidae) in the Acre and Iaco rivers in the western Amazon region of Brazil: diversity, similarity and seasonal variation. J. Nat. Hist. 53(23–24): 1465–1479. Doi: 10.1080/00222933.2019.1657195
» https://doi.org/10.1080/00222933.2019.1657195

[21] ²¹
NEVES, L.R., SILVA, L.M.A., TAVARES DIAS, M. 2021. Diversity and ecology of endohelminth parasites in a fish assemblage of an Amazon River tributary in Brazil. Acta Parasitol. 66:1431–1441. https://doi.org/10.1007/s11686-021-00413-4
» https://doi.org/10.1007/s11686-021-00413-4

[22] ²²
OLIVEIRA, M.S.B., PRESTES, L., ADRIANO, E.A., TAVARES-DIAS, M. 2022. Morphological and functional structure of two Ergasilidae parasites determine their microhabitat affinity on the gills of an Anostomidae fish from the Amazon. Parasitol. Res. 121:2295–2305: https://doi.org/10.1007/s00436-022-07569-6
» https://doi.org/10.1007/s00436-022-07569-6

[23] ²³
PATERSON, R.A., VIOZZI, G.P., RAUQUE, C.A., FLORES, V.R. & POULIN, R. A global Assessment of parasite diversity in galaxiid fishes. Diversity 13:27, 2021. https://doi.org/ 10.3390/d13010027
» https://doi.org/10.3390/d13010027

[24] ²⁴
PAVANELLI, G.C., MACHADO, M.H., TAKEMOTO, R.M., GUIDELLI, G.M. & LIZAMA, M.A.P. 2004. Helminth fauna of fishes: Diversity and ecological aspects. In THOMAZ, SM., AGOSTINHO, AA. & HAHN, NS. The upper Paraná River and its floodplain physical aspects, ecology and conservation. Backhuys Publishers: Leiden. p. 309–329.

[25] ²⁵
PEREIRA, J. O., SILVA M. T., VIEIRA L.J.S & FUGI, R. 2011. Effects of flood regime on the diet Triportheus curtus (Garman, 1890) in an Amazonian floodplain lake. Neotrop. Ichthyol. 9(3):623–628. doi: 10.1590/S1679-62252011005000029
» https://doi.org/10.1590/S1679-62252011005000029

[26] ²⁶
RIGBY, M.C. 2014. 7.20 Order Camallanida: Superfamilies Anguillicoloidea and Camallanoidea. In: SCHMIDT-RHAESA, A (Ed.) Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera: Vol. 2, Nematoda. Walter De Gruyter, Berlin, p. 637–659.

[27] ²⁷
RODRÍGUEZ-ZORRO, P.A., ENTERS, D., HERMANOWSKI B., COSTA, M.L.C. & BEHLING, H. 2015. Vegetation changes and human impact inferred from an oxbow lake in southwestern Amazonia, Brazil since the 19th century. J. South Amer. Earth Sci. 62: 186e194. http://dx.doi.org/10.1016/j.jsames.2015.06.003
» https://doi.org/10.1016/j.jsames.2015.06.003

[28] ²⁸
RÓZSA, L., REICZIGEL, J. & MAJOROS, G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86:228–232.

[29] ²⁹
SILVA, M.T, PEREIRA J.O., SOARES VIEIRA L.J. & PETRY, A.C. 2013. Hydrological seasonality of the river affecting fish community structure of oxbow lakes: A limnological approach on the Amapá Lake, southwestern Amazon. Limnologica 43:79–90. http://dx.doi.org/10.1016/j.limno.2012.05.002
» https://doi.org/10.1016/j.limno.2012.05.002

[30] ³⁰
TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A. & SILVA, L.M.A. 2014. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitol. 59(1): 158–164. Doi: 10.2478/s11686-014-0225-3
» https://doi.org/10.2478/s11686-014-0225-3

[31] ³¹
TAVARES-DIAS, M., DIAS-JÚNIOR, M.B.F., FLORENTINO, A.C., SILVA, L.M.A. & CUNHA, AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Rev. Bras. Parasitol. Vet. 24:136–147. https://doi.org/10.1590/S1984-29612015036
» https://doi.org/10.1590/S1984-29612015036

[32] ³²
TAVARES-DIAS, M., OLIVEIRA, M.S.B., GONÇALVES, R.A., NEVES, L.R. 2017. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amaz. 47(2):155–162. https://doi.org/10.1590/1809-4392201602514
» https://doi.org/10.1590/1809-4392201602514

[33] ³³
THATCHER, V.E. Amazon Fish Parasites. Pensoft: Sofia Moscow.

[34] ³⁴
VIRGILIO, L.R., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. 2021. Endofauna of helminth parasites of fish in the Amazon basin. SAJEBTT, 8(1):102–116.

[35] ³⁵
VIRGILIO, L.R., MARTINS, W.M.O., LIMA, F.S., TAKEMOTO, R.M., CAMARGO, L.M.A. & MENEGUETTI, D.U.O. (2022). Endoparasite fauna of freshwater fish from the upper Juruá River in the Western Amazon, Brazil. J. Helminthol. 96: e55, 1–27. https://doi.org/10.1017/S0022149X2200027X
» https://doi.org/10.1017/S0022149X2200027X

[36] ³⁶
WILLIAMS, E.H. & BUNKLEY-WILLIAMS, L. 2019. Life Cycle and life history strategies of parasitic Crustacea. In: SMIT, N., BRUCE, N. & HADFIELD, K. (eds). Parasitic Crustacea. Zoological Monographs, vol 3. Springer, p 179–266.

[37] ³⁷
ZAR, J.H. 2010. Biostatistical analysis. 5th ed. Prentice Hall, New Jersey.

Fish species	Family	N	Weight (g)	Length (cm)	Trophic level^* * Based on Froese and Pauly (2023).	Main feeding items^* * Based on Froese and Pauly (2023).
Curimata inornata Vari, 1989	Curimatidae	8	74.3 ± 13.9	18.2 ± 1.2	Detritivorous	Zoobenthos, algae and detritus
Curimatella meyeri Steindachner, 1882	Curimatidae	13	124.5 ± 37.7	18.2 ± 1.3	Detritivorous	Detritus and aquatic plants
Potamorhina latior Spix & Agassiz, 1829	Curimatidae	31	82.5 ± 22.4	18.6 ± 2.5	Detritivorous	Detritus and aquatic plant
Psectrogaster rutiloides Kner, 1858	Curimatidae	8	76.3 ± 18.1	16.2 ± 1.1	Detritivorous	Detritus, aquatic plants and periphyton
Rhaphiodon vulpinus Spix & Agassiz, 1829	Cynodontidae	13	191.1 ± 96.5	34.9 ± 4.0	Omnivorous	Nekton and fish
Hypophthalmus marginatus Valenciennes, 1840	Pimelodidae	34	269.3 ± 69.3	33.2 ± 4.9	Omnivorous	Zooplankton and invertebrates
Nemadoras humeralis Kner, 1855	Doradidae	19	43.3 ± 15.4	14.3 ± 0.6	Omnivorous	Detritus, aquatic plants, invertebrates, crustacean and fish
Auchenipterus nuchalis Spix & Agassiz, 1829	Auchenipteridae	15	78.0 ± 14.7	19.8 ± 1.2	Omnivorous	Zoobenthos, nekton, insects, invertebrates, crustacean and fish
Pimelodus blochii Valenciennes, 1840	Pimelodidae	14	63.2 ± 40.1	19.6 ± 3.1	Omnivorous	Zoobenthos, nekton, detritus, aquatic plants, insects, invertebrates, crustacean and fish
Sorubim lima Bloch & Schneider, 1801	Pimelodidae	4	73.8 ± 24.7	27.0 ± 2.8	Omnivorous	Zoobenthos, nekton, detritus, aquatic plants, insects, invertebrates, crustacean and fish

Host species	Parasite species	P (%)	MI	MA	TNP	Infection site
Psectrogaster rutiloides	–	0	0	–	–	–
Curimata inornata	Proterodiplostomidae gen. sp. (metacercariae)	37.5	42.0	15.8	126	Intestine
	Ergasilus jaraquensis^{Thatcher & Robertson, 1982}33 THATCHER, V.E. Amazon Fish Parasites. Pensoft: Sofia Moscow. #	12.5	1.0	0.1	1	Gills
Curimatella meyeri	Dactylogyridae gen. sp.1	23.1	2.0	0.5	6	Gills
	Dactylogyridae gen. sp.2	7.1	1.0	0.08	1	Gills
Potamorhina latior	Dactylogyridae gen. sp.1	3.2	2.0	0.1	2	Gills
	Dactylogyridae gen. sp.2	22.6	2.4	0.5	17	Gills
	Dactylogyridae gen. sp.3	9.7	2.7	0.3	8	Gills
	Dactylogyridae gen. sp.4	6.6	1.0	0.06	2	Gills
	Anacanthorus spathulatus Kritsky, Boeger & Van Every, 1992#	9.7	9.7	0.9	29	Gills
	Anacanthorus thatcheri Boeger & Kritsky 1988 #	3.2	1.0	0.03	1	Gills
	Anacanthorus sp.#	3.2	1.0	0.03	1	Gills
	Rhinoxenus sp.#	3.2	1.0	0.03	1	Gills
	Proterodiplostomidae gen. sp. and Diplostomidae gen. sp. (metacercariae)	67.7	56.2	38.1	1181	Intestine
	Anisakidae gen. sp. (larvae)	6.5	3.0	0.2	6	Liver
	Miracetyma etimaruya Malta, 1993	14.3	3.0	0.3	9	Gills
Rhaphiodon vulpinus	Notozothecium lamotherargumedoi Cohen & Kohn, 2008	100	42.5	43.5	553	Gills
	Digenea gen. sp. (metacercariae)	7.7	7.0	0.5	7	Intestine
	Eustrongylides sp. (larvae)#	7.7	3.0	0.2	3	Intestine
	Contracaecum sp.L3 (larvae)	7.7	3.0	0.2	3	Liver
	Terranova sp. L3 (larvae)#	30.8	13.0	4.0	52	Intestine
	Spirocamallanus sp.#	7.7	1.0	0.1	1	Intestine
	Pseudoproleptus sp. (larvae)#	7.7	28.0	2.2	28	Intestine
	Anisakidae gen. sp. (larvae)	7.7	19.0	1.5	19	Intestine
	Ergasilus tipurus Varella, Morey & Malta, 2019	46.2	5.5	2.2	33	Gills
	Miracetyma kawa Malta, 1994	7.7	4.0	3.0	4	Gills
Hypophthalmus marginatus	Dactylogyridae gen. sp.1	2.9	8.0	0.2	8	Gills
	Dactylogyridae gen. sp.2	5.9	3.0	0.2	6	Gills
	Ameloblastella edentensis Mendoza-Franco, Mendoza-Palmero & Scholz, 2016 #	79.4	57.2	43.8	1484	Gills
	Ameloblastella martinae Mendoza-Palmero, Rossin, Irigoitia & Scholz, 2020 #	5.9	4.0	0.2	8	Gills
	Ameloblastella peruensis Mendoza-Franco, Mendoza-Palmero & Scholz, 2016#	8.7	4.5	0.3	9	Gills
	Digenea gen. sp. (metacercariae)	14.7	5.4	0.8	27	Intestine
	Contracaecum sp.L3 (larvae)#	20.6	33.2	7.8	266	Intestine
	Anisakidae gen.sp. (larvae)	14.7	12.4	1.9	62	Liver
	Terranova sp. L3 (larvae)#	5.9	11.5	0.7	23	Abdominal cavity
	Neochinorhynchus sp. (larvae)	32.4	11.7	3.9	129	Intestine
	Miracetymasp.#	73.5	23.8	28.0	595	Gills
Nemadoras humeralis	Cosmetocleithrum sp.1#	10.5	11.5	1.2	23	Gills
	Cosmetocleithrum sp.2#	10.5	2.0	0.1	2	Gills
	Dactylogyridae gen. sp.	10.5	2.0	0.1	2	Gills
	Rhipidocotyle sp. and Proterodiplostomidae gen. sp.#	31.6	9.2	2.9	55	Intestine
	Anisakidae gen. sp. (larvae)#	63.9	2.2	1.4	27	Intestine
	Isopoda gen. sp.	5.3	1.0	0.05	1	Gills
Pimelodus blochii	Ameloblastella amazonica Negreiros, Tavares-Dias & Pereira, 2019	7.1	31.0	2.2	31	Gills
	Ameloblastella satoi Monteiro, Kritsky & Brasil-Sato, 2010#	7.1	3.0	0.2	3	Gills
	Demidospermus striatus Mendoza-Palmero & Scholz, 2011	7.1	4.0	0.3	4	Gills
	Demidospermus leptosynophalus Kritsky & Gutiérrez, 1996	7.1	2.0	0.1	2	Gills
	Demidospermus peruvianus Mendoza-Palmero & Scholz, 2011	7.1	56.0	4.0	56	Gills
	Digenea gen. sp. (metacercariae)	7.1	1.0	0.07	1	Intestine
	Prosthenhystera obesa Diesing, 1850	7.1	1.0	0.07	1	Intestine
	Dadaytrema oxycephalum Diesing, 1850	21.4	14.0	2.9	42	Intestine
	Anisakidae gen. sp. (larvae)	28.6	8.7	2.5	35	Intestine
	Philometroide acreanensis Cavalcante, Moravec & Santos, 2017	7.1	2.0	0.1	2	Intestine
	Spirocamallanus pimelodus Pinto, Fabio, Noronha & Rolas, 1976	14.3	9.5	1.4	19	Intestine
	Ergasilus sp.	35.7	5.4	1.9	27	Gills
Sorubim lima	Digenea gen. sp. (metacercariae)	75.0	11.0	8.2	33	Intestine
	Anisakidae gen. sp. (larvae)	100	21.0	21.0	84	Intestine
Auchenipterus nuchalis	Diplostomidae gen. sp. (metacercariae)	6.7	46.0	3.1	46	Intestine
	Neochinorhynchus sp. (larvae) #	73.3	4.1	3.0	45	Intestine
	Spirocamallanus sp. (larvae) #	40	1.3	0.5	8	Intestine

Host species	Parasite species	DI	d	D	Type of dispersion
Potamorhina latior	Monogeneans	1.848	2.345	0.668	Aggregated
Potamorhina latior	Proterodiplostomidae gen. sp. and Diplostomidae gen. sp.	3.639	6.591	0.494	Aggregated
Hypophthalmus marginatus	Monogeneans	3.052	6.007	0.429	Aggregated
Hypophthalmus marginatus	Digenea gen. sp.	2.04	3.418	0.838	Aggregated
Hypophthalmus marginatus	Contracaecum sp. L3	2.854	5.539	0.707	Aggregated
Hypophthalmus marginatus	Anisakidae gen. sp.	2.04	3.418	0.838	Aggregated
Hypophthalmus marginatus	Miracetymasp.	2.737	5.535	0.497	Aggregated

Host species	Parasite species	Weight		Length
Host species	Parasite species	rs	p	rs	p
Curimata inornata	Proterodiplostomidae gen. sp.	0.151	0.721	0.731	0.039
Curimatella meyeri	Dactylogyridae gen. sp. 1 and 2	0.098	0.751	0.124	0.686
Hypophthalmus marginatus	Monogeneans	0.631	0.0001	0.258	0.14
Hypophthalmus marginatus	Nematodes	0.054	0.762	0.249	0.156
Hypophthalmus marginatus	Miracetymasp.	0.639	0.0001	–0.11	0.534
Potamorhina latior	Monogeneans	0.531	0.777	0.099	0.596
Potamorhina latior	Proterodiplostomidae gen. sp. and Diplostomidae gen. sp. (metacercariae)	–0.349	0.045	–0.373	0.039
Potamorhina latior	Miracetyma etimaruya	0.038	0.841	–0.037	0.844
Rhaphiodon vulpinus	Notozothecium lamotherargumedoi	0.391	0.186	0.597	0.031
Rhaphiodon vulpinus	Terranova sp. L3	0.051	0.887	0.037	0.903
Rhaphiodon vulpinus	Ergasilus tipurus	0.014	0.965	–0.419	0.154
Nemadoras humeralis	Diplostomum sp.	–0.17	0.486	0.022	0.93
Nemadoras humeralis	Anisakidae gen. sp	–0.435	0.063	–0.128	0.612

Brasil

Brasil

Metazoan parasite fauna of detritivorous and omnivorous fishes from Amapá Lake, in western Brazilian Amazon

Fauna parasitária de metazoários em peixes detritívoros e onívoros do Lago Amapá, na Amazônia Ocidental brasileira

Abstract

Resumo

Introduction

Material and Methods

Results

Discussion

Acknowledgements

Data Availability

References

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Publication Dates

History